Subsets of exhausted CD8+ T cells differentially mediate tumor control and respond to checkpoint blockade

T cell dysfunction is a hallmark of many cancers, but the basis for T cell dysfunction and the mechanisms by which antibody blockade of the inhibitory receptor PD-1 (anti-PD-1) reinvigorates T cells are not fully understood. Here we show that such therapy acts on a specific subpopulation of exhauste...

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Published in:	Nature immunology Vol. 20; no. 3; pp. 326 - 336
Main Authors:	Miller, Brian C., Sen, Debattama R., Al Abosy, Rose, Bi, Kevin, Virkud, Yamini V., LaFleur, Martin W., Yates, Kathleen B., Lako, Ana, Felt, Kristen, Naik, Girish S., Manos, Michael, Gjini, Evisa, Kuchroo, Juhi R., Ishizuka, Jeffrey J., Collier, Jenna L., Griffin, Gabriel K., Maleri, Seth, Comstock, Dawn E., Weiss, Sarah A., Brown, Flavian D., Panda, Arpit, Zimmer, Margaret D., Manguso, Robert T., Hodi, F. Stephen, Rodig, Scott J., Sharpe, Arlene H., Haining, W. Nicholas
Format:	Journal Article
Language:	English
Published:	New York Nature Publishing Group US 01.03.2019 Nature Publishing Group
Subjects:	631/250/1619/554/1834/1269 631/250/2502/2170 631/250/580 692/699/67/1059/2325 Animals Antibodies, Blocking - immunology Antibodies, Blocking - pharmacology Biomedical and Life Sciences Biomedicine CD8 antigen CD8-Positive T-Lymphocytes - drug effects CD8-Positive T-Lymphocytes - immunology CD8-Positive T-Lymphocytes - virology Cell Line, Tumor Chronic infection Cytotoxicity Epigenetics Female Humans Immune checkpoint Immunology Infectious Diseases Lymphocyte Subsets - drug effects Lymphocyte Subsets - immunology Lymphocyte Subsets - virology Lymphocytes Lymphocytes T Lymphocytes, Tumor-Infiltrating - drug effects Lymphocytes, Tumor-Infiltrating - immunology Lymphocytes, Tumor-Infiltrating - virology Lymphocytic Choriomeningitis - immunology Lymphocytic Choriomeningitis - prevention & control Lymphocytic Choriomeningitis - virology Lymphocytic choriomeningitis virus - drug effects Lymphocytic choriomeningitis virus - immunology Lymphocytic choriomeningitis virus - physiology Melanoma Melanoma, Experimental - immunology Melanoma, Experimental - prevention & control Melanoma, Experimental - virology Mice, Congenic Mice, Inbred C57BL PD-1 protein Programmed Cell Death 1 Receptor - antagonists & inhibitors Programmed Cell Death 1 Receptor - immunology Programmed Cell Death 1 Receptor - metabolism Transcription Tumor-infiltrating lymphocytes
ISSN:	1529-2908, 1529-2916, 1529-2916
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Abstract	T cell dysfunction is a hallmark of many cancers, but the basis for T cell dysfunction and the mechanisms by which antibody blockade of the inhibitory receptor PD-1 (anti-PD-1) reinvigorates T cells are not fully understood. Here we show that such therapy acts on a specific subpopulation of exhausted CD8 + tumor-infiltrating lymphocytes (TILs). Dysfunctional CD8 + TILs possess canonical epigenetic and transcriptional features of exhaustion that mirror those seen in chronic viral infection. Exhausted CD8 + TILs include a subpopulation of ‘progenitor exhausted’ cells that retain polyfunctionality, persist long term and differentiate into ‘terminally exhausted’ TILs. Consequently, progenitor exhausted CD8 + TILs are better able to control tumor growth than are terminally exhausted T cells. Progenitor exhausted TILs can respond to anti-PD-1 therapy, but terminally exhausted TILs cannot. Patients with melanoma who have a higher percentage of progenitor exhausted cells experience a longer duration of response to checkpoint-blockade therapy. Thus, approaches to expand the population of progenitor exhausted CD8 + T cells might be an important component of improving the response to checkpoint blockade. Exhausted cytotoxic T lymphocytes (CTLs) express the receptor PD-1 as a key signature. Haining and colleagues show that there are different ‘depths’ of exhaustion with a subset of exhausted CTLs that retain polyfunctionality and are responsive to PD-1 blockade.
AbstractList	T cell dysfunction is a hallmark of many cancers, but the basis for T cell dysfunction and the mechanisms by which antibody blockade of the inhibitory receptor PD-1 (anti-PD-1) reinvigorates T cells are not fully understood. Here we show that such therapy acts on a specific subpopulation of exhausted CD8+ tumor-infiltrating lymphocytes (TILs). Dysfunctional CD8+ TILs possess canonical epigenetic and transcriptional features of exhaustion that mirror those seen in chronic viral infection. Exhausted CD8+ TILs include a subpopulation of ‘progenitor exhausted’ cells that retain polyfunctionality, persist long term and differentiate into ‘terminally exhausted’ TILs. Consequently, progenitor exhausted CD8+ TILs are better able to control tumor growth than are terminally exhausted T cells. Progenitor exhausted TILs can respond to anti-PD-1 therapy, but terminally exhausted TILs cannot. Patients with melanoma who have a higher percentage of progenitor exhausted cells experience a longer duration of response to checkpoint-blockade therapy. Thus, approaches to expand the population of progenitor exhausted CD8+ T cells might be an important component of improving the response to checkpoint blockade.Exhausted cytotoxic T lymphocytes (CTLs) express the receptor PD-1 as a key signature. Haining and colleagues show that there are different ‘depths’ of exhaustion with a subset of exhausted CTLs that retain polyfunctionality and are responsive to PD-1 blockade. T cell dysfunction is a hallmark of many cancers, but the basis for T cell dysfunction and the mechanisms by which antibody blockade of the inhibitory receptor PD-1 (anti-PD-1) reinvigorates T cells are not fully understood. Here we show that such therapy acts on a specific subpopulation of exhausted CD8+ tumor-infiltrating lymphocytes (TILs). Dysfunctional CD8+ TILs possess canonical epigenetic and transcriptional features of exhaustion that mirror those seen in chronic viral infection. Exhausted CD8+ TILs include a subpopulation of ‘progenitor exhausted’ cells that retain polyfunctionality, persist long term and differentiate into ‘terminally exhausted’ TILs. Consequently, progenitor exhausted CD8+ TILs are better able to control tumor growth than are terminally exhausted T cells. Progenitor exhausted TILs can respond to anti-PD-1 therapy, but terminally exhausted TILs cannot. Patients with melanoma who have a higher percentage of progenitor exhausted cells experience a longer duration of response to checkpoint-blockade therapy. Thus, approaches to expand the population of progenitor exhausted CD8+ T cells might be an important component of improving the response to checkpoint blockade. T cell dysfunction is a hallmark of many cancers, but the basis for T cell dysfunction and the mechanisms by which antibody blockade of the inhibitory receptor PD-1 (anti-PD-1) reinvigorates T cells are not fully understood. Here we show that such therapy acts on a specific subpopulation of exhausted CD8+ tumor-infiltrating lymphocytes (TILs). Dysfunctional CD8+ TILs possess canonical epigenetic and transcriptional features of exhaustion that mirror those seen in chronic viral infection. Exhausted CD8+ TILs include a subpopulation of 'progenitor exhausted' cells that retain polyfunctionality, persist long term and differentiate into 'terminally exhausted' TILs. Consequently, progenitor exhausted CD8+ TILs are better able to control tumor growth than are terminally exhausted T cells. Progenitor exhausted TILs can respond to anti-PD-1 therapy, but terminally exhausted TILs cannot. Patients with melanoma who have a higher percentage of progenitor exhausted cells experience a longer duration of response to checkpoint-blockade therapy. Thus, approaches to expand the population of progenitor exhausted CD8+ T cells might be an important component of improving the response to checkpoint blockade.T cell dysfunction is a hallmark of many cancers, but the basis for T cell dysfunction and the mechanisms by which antibody blockade of the inhibitory receptor PD-1 (anti-PD-1) reinvigorates T cells are not fully understood. Here we show that such therapy acts on a specific subpopulation of exhausted CD8+ tumor-infiltrating lymphocytes (TILs). Dysfunctional CD8+ TILs possess canonical epigenetic and transcriptional features of exhaustion that mirror those seen in chronic viral infection. Exhausted CD8+ TILs include a subpopulation of 'progenitor exhausted' cells that retain polyfunctionality, persist long term and differentiate into 'terminally exhausted' TILs. Consequently, progenitor exhausted CD8+ TILs are better able to control tumor growth than are terminally exhausted T cells. Progenitor exhausted TILs can respond to anti-PD-1 therapy, but terminally exhausted TILs cannot. Patients with melanoma who have a higher percentage of progenitor exhausted cells experience a longer duration of response to checkpoint-blockade therapy. Thus, approaches to expand the population of progenitor exhausted CD8+ T cells might be an important component of improving the response to checkpoint blockade. T cell dysfunction is a hallmark of many cancers, but the basis for T cell dysfunction and the mechanisms by which antibody blockade of the inhibitory receptor PD-1 (anti-PD-1) reinvigorates T cells are not fully understood. Here we show that such therapy acts on a specific subpopulation of exhausted CD8 tumor-infiltrating lymphocytes (TILs). Dysfunctional CD8 TILs possess canonical epigenetic and transcriptional features of exhaustion that mirror those seen in chronic viral infection. Exhausted CD8 TILs include a subpopulation of 'progenitor exhausted' cells that retain polyfunctionality, persist long term and differentiate into 'terminally exhausted' TILs. Consequently, progenitor exhausted CD8 TILs are better able to control tumor growth than are terminally exhausted T cells. Progenitor exhausted TILs can respond to anti-PD-1 therapy, but terminally exhausted TILs cannot. Patients with melanoma who have a higher percentage of progenitor exhausted cells experience a longer duration of response to checkpoint-blockade therapy. Thus, approaches to expand the population of progenitor exhausted CD8 T cells might be an important component of improving the response to checkpoint blockade. T cell dysfunction is a hallmark of many cancers, but the basis for T cell dysfunction and the mechanisms by which antibody blockade of the inhibitory receptor PD-1 (anti-PD-1) reinvigorates T cells are not fully understood. Here we show that such therapy acts on a specific subpopulation of exhausted CD8 + tumor-infiltrating lymphocytes (TILs). Dysfunctional CD8 + TILs possess canonical epigenetic and transcriptional features of exhaustion that mirror those seen in chronic viral infection. Exhausted CD8 + TILs include a subpopulation of ‘progenitor exhausted’ cells that retain polyfunctionality, persist long term and differentiate into ‘terminally exhausted’ TILs. Consequently, progenitor exhausted CD8 + TILs are better able to control tumor growth than are terminally exhausted T cells. Progenitor exhausted TILs can respond to anti-PD-1 therapy, but terminally exhausted TILs cannot. Patients with melanoma who have a higher percentage of progenitor exhausted cells experience a longer duration of response to checkpoint-blockade therapy. Thus, approaches to expand the population of progenitor exhausted CD8 + T cells might be an important component of improving the response to checkpoint blockade. Exhausted cytotoxic T lymphocytes (CTLs) express the receptor PD-1 as a key signature. Haining and colleagues show that there are different ‘depths’ of exhaustion with a subset of exhausted CTLs that retain polyfunctionality and are responsive to PD-1 blockade.
Author	Panda, Arpit Hodi, F. Stephen Sharpe, Arlene H. Collier, Jenna L. LaFleur, Martin W. Manguso, Robert T. Ishizuka, Jeffrey J. Haining, W. Nicholas Bi, Kevin Brown, Flavian D. Al Abosy, Rose Sen, Debattama R. Felt, Kristen Kuchroo, Juhi R. Weiss, Sarah A. Zimmer, Margaret D. Lako, Ana Manos, Michael Rodig, Scott J. Naik, Girish S. Comstock, Dawn E. Griffin, Gabriel K. Yates, Kathleen B. Virkud, Yamini V. Miller, Brian C. Gjini, Evisa Maleri, Seth
AuthorAffiliation	3 Broad Institute of MIT and Harvard, Cambridge, MA, USA 4 Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA, USA 6 Division of Medical Sciences, Harvard Medical School, Boston, MA, USA 10 These authors contributed equally: Brian C. Miller, Debattama R. Sen 8 Center for Immuno-Oncology, Dana-Farber Cancer Institute, Boston, MA, USA 9 Department of Pathology, Brigham and Women’s Hospital, Boston, MA, USA 1 Department of Pediatric Oncology, Dana-Farber Cancer Institute, Boston, MA, USA 5 Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA 7 Division of Pediatric Allergy and Immunology, Massachusetts General Hospital, Boston, MA, USA 2 Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA, USA
AuthorAffiliation_xml	– name: 2 Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA, USA – name: 5 Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA – name: 10 These authors contributed equally: Brian C. Miller, Debattama R. Sen – name: 1 Department of Pediatric Oncology, Dana-Farber Cancer Institute, Boston, MA, USA – name: 3 Broad Institute of MIT and Harvard, Cambridge, MA, USA – name: 9 Department of Pathology, Brigham and Women’s Hospital, Boston, MA, USA – name: 7 Division of Pediatric Allergy and Immunology, Massachusetts General Hospital, Boston, MA, USA – name: 4 Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA, USA – name: 6 Division of Medical Sciences, Harvard Medical School, Boston, MA, USA – name: 8 Center for Immuno-Oncology, Dana-Farber Cancer Institute, Boston, MA, USA
Author_xml	– sequence: 1 givenname: Brian C. orcidid: 0000-0001-5931-4184 surname: Miller fullname: Miller, Brian C. organization: Department of Pediatric Oncology, Dana-Farber Cancer Institute, Department of Medical Oncology, Dana-Farber Cancer Institute, Broad Institute of MIT and Harvard, Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Department of Immunology, Blavatnik Institute, Harvard Medical School – sequence: 2 givenname: Debattama R. orcidid: 0000-0002-0947-8284 surname: Sen fullname: Sen, Debattama R. organization: Department of Pediatric Oncology, Dana-Farber Cancer Institute, Broad Institute of MIT and Harvard, Division of Medical Sciences, Harvard Medical School – sequence: 3 givenname: Rose orcidid: 0000-0001-5400-1306 surname: Al Abosy fullname: Al Abosy, Rose organization: Department of Pediatric Oncology, Dana-Farber Cancer Institute, Broad Institute of MIT and Harvard – sequence: 4 givenname: Kevin surname: Bi fullname: Bi, Kevin organization: Department of Pediatric Oncology, Dana-Farber Cancer Institute, Broad Institute of MIT and Harvard – sequence: 5 givenname: Yamini V. surname: Virkud fullname: Virkud, Yamini V. organization: Division of Pediatric Allergy and Immunology, Massachusetts General Hospital – sequence: 6 givenname: Martin W. orcidid: 0000-0002-5017-774X surname: LaFleur fullname: LaFleur, Martin W. organization: Department of Pediatric Oncology, Dana-Farber Cancer Institute, Broad Institute of MIT and Harvard, Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Department of Immunology, Blavatnik Institute, Harvard Medical School, Division of Medical Sciences, Harvard Medical School – sequence: 7 givenname: Kathleen B. surname: Yates fullname: Yates, Kathleen B. organization: Department of Pediatric Oncology, Dana-Farber Cancer Institute, Broad Institute of MIT and Harvard – sequence: 8 givenname: Ana surname: Lako fullname: Lako, Ana organization: Center for Immuno-Oncology, Dana-Farber Cancer Institute – sequence: 9 givenname: Kristen surname: Felt fullname: Felt, Kristen organization: Center for Immuno-Oncology, Dana-Farber Cancer Institute – sequence: 10 givenname: Girish S. surname: Naik fullname: Naik, Girish S. organization: Center for Immuno-Oncology, Dana-Farber Cancer Institute – sequence: 11 givenname: Michael surname: Manos fullname: Manos, Michael organization: Department of Medical Oncology, Dana-Farber Cancer Institute, Center for Immuno-Oncology, Dana-Farber Cancer Institute – sequence: 12 givenname: Evisa surname: Gjini fullname: Gjini, Evisa organization: Department of Medical Oncology, Dana-Farber Cancer Institute, Center for Immuno-Oncology, Dana-Farber Cancer Institute – sequence: 13 givenname: Juhi R. surname: Kuchroo fullname: Kuchroo, Juhi R. organization: Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Department of Immunology, Blavatnik Institute, Harvard Medical School, Division of Medical Sciences, Harvard Medical School – sequence: 14 givenname: Jeffrey J. surname: Ishizuka fullname: Ishizuka, Jeffrey J. organization: Department of Pediatric Oncology, Dana-Farber Cancer Institute, Department of Medical Oncology, Dana-Farber Cancer Institute, Broad Institute of MIT and Harvard – sequence: 15 givenname: Jenna L. orcidid: 0000-0002-4071-4986 surname: Collier fullname: Collier, Jenna L. organization: Department of Pediatric Oncology, Dana-Farber Cancer Institute, Broad Institute of MIT and Harvard, Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Department of Immunology, Blavatnik Institute, Harvard Medical School, Division of Medical Sciences, Harvard Medical School – sequence: 16 givenname: Gabriel K. surname: Griffin fullname: Griffin, Gabriel K. organization: Department of Pediatric Oncology, Dana-Farber Cancer Institute, Broad Institute of MIT and Harvard, Department of Pathology, Brigham and Women’s Hospital – sequence: 17 givenname: Seth surname: Maleri fullname: Maleri, Seth organization: Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Department of Immunology, Blavatnik Institute, Harvard Medical School – sequence: 18 givenname: Dawn E. surname: Comstock fullname: Comstock, Dawn E. organization: Department of Pediatric Oncology, Dana-Farber Cancer Institute, Broad Institute of MIT and Harvard, Division of Medical Sciences, Harvard Medical School – sequence: 19 givenname: Sarah A. surname: Weiss fullname: Weiss, Sarah A. organization: Department of Pediatric Oncology, Dana-Farber Cancer Institute, Broad Institute of MIT and Harvard, Division of Medical Sciences, Harvard Medical School – sequence: 20 givenname: Flavian D. surname: Brown fullname: Brown, Flavian D. organization: Department of Pediatric Oncology, Dana-Farber Cancer Institute, Broad Institute of MIT and Harvard, Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Department of Immunology, Blavatnik Institute, Harvard Medical School, Division of Medical Sciences, Harvard Medical School – sequence: 21 givenname: Arpit surname: Panda fullname: Panda, Arpit organization: Department of Pediatric Oncology, Dana-Farber Cancer Institute, Broad Institute of MIT and Harvard – sequence: 22 givenname: Margaret D. surname: Zimmer fullname: Zimmer, Margaret D. organization: Broad Institute of MIT and Harvard – sequence: 23 givenname: Robert T. surname: Manguso fullname: Manguso, Robert T. organization: Broad Institute of MIT and Harvard – sequence: 24 givenname: F. Stephen surname: Hodi fullname: Hodi, F. Stephen organization: Department of Medical Oncology, Dana-Farber Cancer Institute, Center for Immuno-Oncology, Dana-Farber Cancer Institute – sequence: 25 givenname: Scott J. surname: Rodig fullname: Rodig, Scott J. organization: Center for Immuno-Oncology, Dana-Farber Cancer Institute, Department of Pathology, Brigham and Women’s Hospital – sequence: 26 givenname: Arlene H. surname: Sharpe fullname: Sharpe, Arlene H. organization: Broad Institute of MIT and Harvard, Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Department of Immunology, Blavatnik Institute, Harvard Medical School, Division of Medical Sciences, Harvard Medical School – sequence: 27 givenname: W. Nicholas orcidid: 0000-0001-7871-3762 surname: Haining fullname: Haining, W. Nicholas email: wnhaining@gmail.com organization: Department of Pediatric Oncology, Dana-Farber Cancer Institute, Broad Institute of MIT and Harvard, Division of Medical Sciences, Harvard Medical School
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/30778252$$D View this record in MEDLINE/PubMed
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 J.J.I., J.L.C., A.P., S.M., D.E.C., S.A.W. and F.D.B. performed mouse experiments and/or data analysis. M.D.Z., R.T.M. and F.S.H. provided critical reagents. A.L., K.F., G.S.N., M.M., E.G., G.K.G., F.S.H. and S.J.R. collected human samples and data. B.C.M., D.R.S. and W.N.H. wrote the manuscript. All authors reviewed and edited the manuscript. B.C.M., D.R.S. and W.N.H. conceived the study. B.C.M., D.R.S., A.H.S. and W.N.H. designed the experiments. B.C.M., D.R.S., R.A.A., K.B., Y.V.V., M.W.L., K.B.Y., J.R.K. Author contributions
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Snippet	T cell dysfunction is a hallmark of many cancers, but the basis for T cell dysfunction and the mechanisms by which antibody blockade of the inhibitory receptor...
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SubjectTerms	631/250/1619/554/1834/1269 631/250/2502/2170 631/250/580 692/699/67/1059/2325 Animals Antibodies, Blocking - immunology Antibodies, Blocking - pharmacology Biomedical and Life Sciences Biomedicine CD8 antigen CD8-Positive T-Lymphocytes - drug effects CD8-Positive T-Lymphocytes - immunology CD8-Positive T-Lymphocytes - virology Cell Line, Tumor Chronic infection Cytotoxicity Epigenetics Female Humans Immune checkpoint Immunology Infectious Diseases Lymphocyte Subsets - drug effects Lymphocyte Subsets - immunology Lymphocyte Subsets - virology Lymphocytes Lymphocytes T Lymphocytes, Tumor-Infiltrating - drug effects Lymphocytes, Tumor-Infiltrating - immunology Lymphocytes, Tumor-Infiltrating - virology Lymphocytic Choriomeningitis - immunology Lymphocytic Choriomeningitis - prevention & control Lymphocytic Choriomeningitis - virology Lymphocytic choriomeningitis virus - drug effects Lymphocytic choriomeningitis virus - immunology Lymphocytic choriomeningitis virus - physiology Melanoma Melanoma, Experimental - immunology Melanoma, Experimental - prevention & control Melanoma, Experimental - virology Mice, Congenic Mice, Inbred C57BL PD-1 protein Programmed Cell Death 1 Receptor - antagonists & inhibitors Programmed Cell Death 1 Receptor - immunology Programmed Cell Death 1 Receptor - metabolism Transcription Tumor-infiltrating lymphocytes
Title	Subsets of exhausted CD8+ T cells differentially mediate tumor control and respond to checkpoint blockade
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